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Embryonic Development (Embryogenesis/Gastrulation/Transcription/Coupled Translation-Glycosylation) JOSEPH T

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Embryonic Development (Embryogenesis/Gastrulation/Transcription/Coupled Translation-Glycosylation) JOSEPH T Proc. Natl Acad. Sci. USA Vol. 80, pp. 1028-1032, February 1983 Developmental Biology Regulation of sea urchin glycoprotein mRNAs during embryonic development (embryogenesis/gastrulation/transcription/coupled translation-glycosylation) JOSEPH T. Y. LAU AND WILLIAM J. LENNARZ Department of Physiological Chemistry, The Johns Hopkins University School of Medicin6,i725 N. Wolfe Street, Baltimore, Maryland 21205 Communicated by Daniel Nathans, November 8, 1982 ABSTRACT Gastrulation in sea urchin embryos is accom- which the oligosaccharide is preassembled, and the rate of dol- panied by a striking increase in the synthesis of N-linked glyco- ichol phosphorylation (7) are increased after fertilization. proteins, and inhibitors of this process block gastrulation. In this Presently, nothing is known about the mRNAs that code for report, the messages coding for N-glycosylatable proteins in the glycoproteins in sea urchin embryos. The synthesis of these developing embryo of the sea urchin, Strongylocentrotus purpur- messages and their mobilization into active polysomes may be atmu, were examined. Total mRNAand mRNA isolated from mem- important regulatory points in the activation of glycoprotein branes of the embryos at various stages of development were used synthesis during gastrulation. What is known is that the unfer- to program a cell-free translation/glycosylation system-prepared tilized sea urchin egg contains a vast store of mRNA, which is from rabbit reticulocyte lysate supplemented with dog pancreas microsomes. The glycosylated translation products were sepa- thought to contain all of the information necessary for the early rated from the nonglycosylated products by concanavalin A-agar- development of the embryo (8-11). After fertilization, the stored ose and analyzed by gel electrophoresis. The results indicate that maternal mRNA is activated by an unknown mechanism and then although the RNA derived from the membranes of gastrula-stage mobilized into the polysomes (10). Although synthesis of mRNA embryos contains messages coding fornumerous glycoproteins, only begins shortly after fertilization, it has been suggested on the trace amounts of glycoprotein messages are associated with mem- basis of experiments' with actinomycin D to inhibit RNA syn- branes at earlier stages of development. mRNAs coding for four thesis that gastrulation represents the first stage requiring de glycoproteins of Mrs 70,000, 65,000, 51,000, and 30,000 were ex- novo RNA synthesis (for a review, see ref. 12). amined, further in total RNA preparations from the developing Because glycoproteins apparently need to be synthesized in embryo. The data indicate that the messages coding for the gly- order for the embryos to gastrulate (2-4), it was of interest to coproteins of Mrs 65,000 and 51,000 are present also in the un- examine the mRNAs coding for these glycoproteins to deter- fertilized egg and in the pregastrulation embryo. Because these mine if the messages are synthesized de novo or are maternal two messages are not found associated with the membranes until in origin and stored until gastrulation. Earlier studies have es- *gastrula stage, it is likely that the-synthesis of these glycoproteins tablished that a cell-free translation system supplemented with duringgastrulation is regulated atthe translationallevel. The mes- dog pancreas microsomes faithfully translates and glycosylates sages coding for glycoproteins of Mrs 70,000 and 30,000, on the proteins when.presented with the appropriate mRNA (13-15). other-hand, are not detectable in the unfertilized egg and may be In the currentstudy, glycoproteins synthesized invitro with un- synthesized de novo by the embryos. Thus, the expression of these fractionated sea urchin embryo RNA as message have been sep- two glycoproteins during gastrulation is regulated at least in part arated from the nonglycosylated translation products by con- on the transcriptional level. On the basis of these findings, it ap- canavalin A (Con A)-agarose and analyzed by NaDodSO4 gel pears thatdifferent modes of regulation are used fordifferent gly- electrophoresis. In this manner, total and membrane-associated coproteins that are synthesized during gastrulation. mRNA at various stages of development have been assayed for the presence of messages coding for N-glycosylatable proteins. Gastrulation in the developing embryo is a major morphoge- Wefirstexamined membrane-associated RNAfrom gastrula-stage netic event that requires coordinated cell migration and differ- embryos, a fraction that should contain the actively translating entiation. In sea urchin embryos that have developed to the glycoprotein messages. This RNA was found to be capable of mesenchyme blastula stage, the gastrulation process begins with programming the cell-free synthesis of numerous glycopro- invagination of the ectodermal cell layer near the vegetal pole. teins. Examination ofmembrane-associated RNAfrom embryos Subsequent emergence of proliferating secondary mesenchy- -at earlier stages of development indicates that these messages mal cells and continued invagination eventually leads to the for- are not associated with the membranes until gastrulation. In ad- mation of the primitive gut tube (see ref. 1 for review). Previous dition, the evidence indicates that although two of the glyco- studies from this laboratory have demonstrated that tunica- protein messages are present in the unfertilized egg, two others mycin and compactin, drugs that inhibitNlinked glycosylation, may be synthesized de novo after fertilization. prevent gastrulation without affecting earlier stages of devel- opment (2-5). These observations suggest that gastrulation rep- resents the first developmental stage that,requires newly syn- MATERIALS AND METHODS thesized N-linked glycoproteins. Consistent with these obser- Materials. Sea urchins (Strongylocentrotus purpuratus) were vations, in vivo experiments with [3H]mannose and [3H]glu- purchased from Pacific Biomarine Supply (Venice, CA). The cosamine reveal that the onset ofgastrulationis accompaniedby animals, gametes, and embryos were handled and maintained a dramatic increase in glycoprotein synthesis (2, 5, 6). In ad- as described (2). [3SIMethionine (100GCi/mmol; 1 Ci = 3.7 X dition, the level of dolichyl phosphate (5), the lipid carrier upon 1010 Bq) and D-[2-3H]mannose (18.4 Ci/mmol) were purchased from Amersham. Micrococcal nuclease-treated rabbit reticu- The publication costs of this-article were defrayed in partby page charge payment. This article must therefore be hereby marked "advertise- Abbreviations: endo H, endo-pN-acetylglucosaminidase H; Con A, nent" in accordance with 18 U. S. C. §1734 solely to indicate this fact. concanavalin A. 1028 Downloaded by guest on September 23, 2021 Developmental Biology: Lau and Lennarz Proc. Natl. Acad. Sci. USA 80 (1983) 1029 locyte lysate cell-free translation system and Con A-agarose were Con A buffer was added to the beads, incubated for 30 min, and purchased from Bethesda Research Laboratories; endo-,J-N- the buffer was removed. This was repeated four times and the acetylglucosaminidase H (endo H) was from A. Trimble (New a-methylmannoside supernatant fractions were pooled. 2-Mer York State Department of Health, Albany, NY). Fresh dog pan- captoethanol (final concentration, 1%) and cytochrome c as car- creas was obtained from W. Mitzner (The Johns Hopkins Uni- rier protein (60 ug) were added, and the protein was precipi- versity School of Hygiene and Public Health, Baltimore, MD). tated at 20C with 10% trichloroacetic acid for 4 hr. The tri- Isolation of RNA. For the isolation of total cellular RNA, the chloroacetic acid-insoluble pellet was washed three times with embryos were sedimented and washed once in Millipore (0.45- 90% ice-cold acetone and resolubilized in gel electrophoresis ,um pore size) filtered sea water. Packed embryos (1-2 ml) were sample buffer. solubilized in 40 ml of a solution containing 4 M guanidine iso- Other Procedures. For digestion with endo H, samples were thiocyanate as described by Chirgwin et al. (16). The RNA was diluted 1:1 with 0.4% NaDodSO4/1% 2-mercaptoethanol/0.2 purified by centrifugation through a cushion of 5.7 M CsCl as M 2-[N-morpholino]ethanesulfonic acid, pH 5.6/150 units of described by Glisin et aL (17). For the isolation of polysomes and aprotinin per ml and incubated overnight at room temperature membrane-associated RNA, the embryos (Ito 2 ml) were washed in the presence of 8 milliunits of the enzyme per ml. One-di- twice with Millipore-filtered sea water, twice with sterile Ca2+- mensional 10% polyacrylamide/NaDodSO4 gel electrophoresis and Mg2+-free, artificial sea water, and homogenized in 10 ml was performed as described by Laemmli (20) except that the of 10 mM Tris HCI, pH 7.5/10 mM KCI/2.5 mM MgCl2 with degree of crosslinking was halved. Two-dimensional gel elec- 50 strokes of a Dounce homogenizer. The homogenate was ad- trophoresis was carried out as described by O'Farrell (21). justedto 0.6 M sucrose/50 mM Tris HCI, pH 7.5/25mM KCI/2.5 mM MgCl2, and the nuclei were removed by centrifugation at RESULTS 1,000 X g for 10 min. The supernatant was centrifuged at 40,000 x g for 30 min to obtain a membrane fraction and a soluble frac- In Vitro Synthesis of N-linked Glycoproteins Using Gas- tion. To prepare membrane-associated RNA, the membrane trula-Stage mRNA. Because previous studies from this labo- fraction was extracted by using the guanidine isothiocyanate ratory have established that N-linked glycoprotein synthesis is procedure described above. The 40,000 x g soluble fraction was initiated at the onset of gastrulation, we first studied cell-free brought to 0.1% (vol/vol) Nonidet P40, layered on top of a synthesis of glycoproteins using RNA from gastrula-stage em- cushion consisting of 1.6 M sucrose/50mM Tris HCI, pH 7.5/250 bryos (45 hr after fertilization). Initially, RNA isolated from a mM KCI/2.5 mM MgCl2, and centrifuged at 27,000 X g for 3 membrane fraction that would be expected to contain the gly- hr in a SW 28 rotor. The resulting free polysome pellet was used coprotein polysomal messages was used to program in vitro to prepare RNA by the guanidine isothiocyanate method (16, translation reactions.
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